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Hydrogen sulfide and signaling in plants
John T. Hancock1,4, Miroslav Lisjak2, Tihana Teklic2, Ian D. Wilson1 and
Matthew Whiteman3
1 Faculty of Health and Life Sciences, University of the West of England,
Bristol, UK
2 Department of Agroecology, Faculty of agriculture, University of Josip Juraj
Strossmayer, Osijek, Croatia
3 Peninsula Medical School, University of Exeter, Exeter, UK
4: to whom correspondence should be addressed:
Faculty of Health and Life Sciences
University of the West of England
Coldharbour Lane
Bristol
BS16 1QY, UK
[email protected]
Key words: plants; hydrogen sulfide; signaling; nitric oxide; GYY4137; NaSH.
1
Abstract
Several relatively reactive compounds exist which are considered to play
major roles in plant cell signaling. These include reactive oxygen species such
as hydrogen peroxide and nitric oxide (NO). Until recently hydrogen sulfide
(H2S) has commonly been thought of as a phytotoxin, but a growing body of
evidence now points to the fact that H2S may also have a signaling role and
that it should be ranked as an important signal alongside NO and ROS. At
high concentrations H2S will inhibit enzymes such as cytochrome oxidase.
However, at lower concentrations it may act in a more positive manner. A
renewed interest in the role of H2S in biological systems has been evidenced
in the results of research investigating cell signaling in both animals and
plants. The growth and development of plants may be affected, for example,
during the promotion of adventitious root formation. Stomatal closure has also
been shown to be altered by H2S and it has been reported to be involved in
the tolerance of plants to metals such as aluminium and copper. The
treatment of plant cells with H2S affects cysteine and glutathione metabolism
and there is a growing body of evidence to suggest that the presence of H2S
may impact on oxidative stress metabolism and nitric oxide signaling. New
H2S donor molecules are appearing in the literature, such as GYY4137, and
with such new tools the true extent of the role of H2S in the control of plant
signalling will no doubt be unravelled in the future.
2
Review Methodology
This review was written after searches for papers in the following databases:
Pubmed., Science Direct, Google Scholar, Cab Abstracts using the keyword
searches with both UK English and American English Spelling, such as
hydrogen sulphide & hydrogen sulfide, signalling & signaling. In addition we
used the references from within the articles obtained to check for additional
relevant material.
Introduction
It is now well established that many reactive chemicals are involved in the
control of cellular events both in animals and in plants. Such chemicals
include reactive oxygen species (ROS) and reactive nitrogen species (RNS).
Among these the ROS most studied are hydrogen peroxide and superoxide
anions while the RNS investigated include nitric oxide (NO) and peroxynitrite
[1, 2]. However, although considered as a signal in animals [3, 4] hydrogen
sulfide (H2S) should also to be counted in this group of small, sometimes
gaseous compounds which are used by plants to control their physiological
and biochemical activities. In animals H2S has been dubbed the “third
gasotransmitter” [5], the others being NO and carbon monoxide (CO) and
several research groups are now focussing on H2S and its role as a signal in
plants.
3
However, for molecules to be truly counted as signaling components
there are several criteria which must be adhered to and as such ROS and
RNS have been judged. Signaling molecules need to be produced when
required and to move to a site of action where they must be perceived and
subsequently induce cellular responses. Such compounds also need to be
readily removed when no longer required and are often seen to interact with a
variety of other signal molecules so that they readily partake in signaling
cross-talk. Thus, for hydrogen sulfide to be truly counted as a reactive species
signal similar judgements need to be made. This article will review the
generation and perception of and responses of plants to H2S and so consider
whether it can be classed as a plant cell signaling molecule.
The generation of hydrogen sulfide
H2S is a colorless, flammable gas and therefore might not be
considered to be ideal as a signaling molecule. Certainly, these properties
make it difficult to study. That said, in biological systems H2S can be
measured, one approach being based on the formation of methylene blue
from sulfide and N,N-dimethyl-p-phenylenediamine in the presence of Fe3+
and its spectrophotometric detection at 675 nm [6]. This and similar assays
can be applied to detect H2S in plants and their environments.
Plants may be externally exposed to H2S either atmospherically or by
its presence in the rhizosphere. Certainly, anoxic soil [7], such as that found in
marshlands, can generate H2S and as such the roots of plants in these areas
will be so exposed. Other sulfurous compounds will also be present in such
soils. SO42- reducing bacteria such as Desulfovibriao, found in waterlogged
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soils and marshes, can generate sulfite [8] and sulfite levels in marine soils
have been reported to be higher than 1mM [9]. The aerial parts of plants may
often be exposed to atmospheric H2S. H2S is commonly emitted from many
sources such as waste treatment installations [10], agricultural industries [11]
and from geothermal power plants [12]. It has also been found to be at
surprisingly high concentrations in some urban environments with car catalytic
converters being suggested as a potential source [13]. However, the fact that
plants respond to such exogenous sources of H2S does not necessarily
indicate that it has a signaling role. Often, in such contexts, the responses of
the plants are those associated with the aberrant biochemistry of an organism
exposed to toxic levels of this compound. After all, it is for its phytotoxic
effects at high levels that H2S has become well known [14, 15].
To truly be a cell signaling molecule, H2S must be generated by plants
and indeed endogenous production of H2S can be observed. Using a sulfurspecific flame photometric detector, Wilson et al. [16] showed that, among
other plants, cucumber, squash, pumpkin, soybean and cotton were able to
produce volatile sulfur compounds including H2S. Rates of emission were
variable but were up to 10 nmol min-1 for leaves of about 50 cm2. This ability
was described as being light-dependent and when roots were supplied with
sulfate and the plants illuminated the emissions lasted for several hours.
Furthermore, if either the leaves were fed sulfate through their petioles or if
the roots of the plants were mechanically damaged the rate of the H2S
emission was significantly increased. Sekiya et al. [17] also measured H2S
emissions from cucumber (Cucumis sativus) leaf discs given sulfate in the
light, emitting at a rate of 50–100 pmol min-1 cm-2. Again, using cucumber they
5
also reported that young leaves emit much more H2S than mature leaves [18].
The release of H2S from plants has also been confirmed by Rennenberg [19]
who found that pumpkin leaves emitted H2S if supplied with sulfate, sulfite,
cysteine or SO2. Different metabolic pathways were described to account for
the use of the different sulfur sources to produce the H2S in each case.
In animal cells the production of H2S results from the action of two
enzymes involved in the metabolism of cysteine, cystathionine gamma-lyase
and cystathionine beta synthase [5, 20]. In plants it appears that the enzymes
responsible are desulfhydrases. A plastid located cysteine desulfhydrases has
been reported in Arabidopsis [21] while others report the presence of a similar
enzyme in the mitochondria [22]. The levels of such enzymes are not static
and their activity has been shown to increase after, for example, pathogen
challenge [23]. Therefore, there appear to be inducible and regulated
enzymes capable of making H2S and thus, a mechanism for its generation
when required, one criterion that must be met if it is to be considered as a
cellular signal.
Of course H2S acting as a signal may not come from the plant per se.
Animals and bacteria have been shown to generate H2S. For example
microorganisms which are invading plants, such as pathogenic bacteria, may
be able to release H2S [24] which will then affect the activities of the plant.
Bacterial release of H2S having profound effects on animals has been
reported, such as the promotion of IL-8 production from epithelial cells [25]
and therefore such interactions would not be unlikely in plants too.
6
The effects of hydrogen sulfide on plants
Hydrogen sulfide is a reactive and toxic compound and in animals is
well known to be lethal in high doses, causing inhibition of cytochrome
oxidase in the mitochondria [for example 26]. It was found that cytochrome
oxidase in olfactory epithelium was decreased with H2S at a concentration of
30 ppm or above. It is, therefore, not surprising that over a number of years it
has been established that hydrogen sulfide (H2S) may also have similar
effects on plants and that it has generally been thought to be a phytotoxin. For
example, 35 years ago it was described as inhibiting oxygen release from
various cultivars of young rice seedlings [27]. H2S was used at concentrations
of 0.2 to 10 μg mL-1. It was also noted that in some cultivars of rice nutrient
uptake was also reduced, while in other cultivars it was increased.
Phosphorous uptake was also inhibited in this plant species. Thompson and
Kats [28] continuously fumigated various species of plants with H2S. In
Medicago, grape, lettuce, sugar beet, pine and fir 3000 parts per billion (ppb)
H2S caused lesions on the leaves, defoliation and reduced growth of the
plants. However, H2S treatment has not always been shown to be deleterious.
Interestingly, lower levels of fumigation, 100 ppb, caused a significant
increase in the growth of Medicago, lettuce and sugar beet [28]. While
working with beet it was also noted that there was less fungal attack following
H2S treatment, suggesting that the H2S may inhibit the growth of the fungi.
However, H2S was observed to reduce the sugar content of the roots of the
beet plants.
An increase in either the tolerance to or the protection against some
plant stresses has also been found to be mediated by H2S. In a similar
7
manner to the above [19], Hällgren and Fredriksson [29] showed that when
pine (Pinus silvestris L.) needles were subjected to low concentrations of SO2
emissions of H2S could be measured that resulted in an increase in the
tolerance of the plants to the SO2. The emissions were light dependent, lasted
for a considerable time after the SO2 was removed and it was suggested that
sulfur metabolism in the chloroplasts was responsible. A similar example of
H2S-induced SO2 tolerance was seen with young Cucurbitaceae leaves [17].
Takemoto et al. [30] detected increased emission of H2S and thiol
accumulation in duckweed (Lemnaceae) under high irradiance and
hypothesized that this was important for sulfite tolerance.
Much of the work on H2S and its effect on plants was carried out many
years ago. However, more recently there has been a renewed interest. In
2004 Bloem et al. [23] showed that fungal infection, particularly with
Pyrenopeziza brassicae caused an increase in the activity of an enzyme
capable of generating H2S, and thus, a greater potential for H2S release from
the plant being infected. More recently Zhang et al. [31] showed that the H2S
donor NaSH could alleviate the osmotic-induced decrease in chlorophyll
concentration in sweet potato. Furthermore, spraying the plants with NaSH
induced increases in the activities of the antioxidant enzymes superoxide
dismutase, catalase and ascorbate peroxidase and decreases in the
concentration of hydrogen peroxide and the activity of lipoxygenase,
suggesting that H2S has a role in protecting plants against oxidative stress.
Other plant responses linked to H2S include freezing tolerance [32], a process
which also has links to changes in oxidative stress metabolism. Similar H2S
mediated stress tolerance has also been reported in animals [20].
8
Aluminium is known to inhibit seed germination and pre-treatment with
NaSH has been shown to alleviate this in a concentration-dependent manner
with an optimum at 0.3 nmol L-1 [33]. Following NaSH treatment, endogenous
H2S was seen to increase and again the levels of enzymes involved in
oxidative stress were altered. There was a decrease in the activity of
lipoxygenase, but an increase in the activities of catalase, superoxide
dismutase, ascorbate peroxidase and guaiacol peroxidase. Clearly, there
appears to be a link between the presence of H2S and the oxidative stress
responses of plant cells and similarly. NaSH has also been shown to alleviate
the copper inhibition of germination in wheat [34]. In this case, NaSH caused
an increase in superoxide dismutase and catalase activities, decreased
lipoxygenase activity, left the activity of ascorbate peroxidase unchanged,
increased esterase and amylase activities and caused a reduction in
hydrogen peroxide and malondialdehyde levels. Further work in which wheat
seeds were pre-treated with NaSH for 12 h showed that H2S preferentially
affected the activity of endosperm β-amylase and that the synthesis and
activity of α-amylase remained unaffected [35]. However, overall such studies
highlight the probable interaction of H2S and ROS metabolism.
Intracellular responses to hydrogen sulfide
It has been suggested that H2S is a signaling molecule in animals [3-5,
36-38] and that it is likely, therefore, that the same is true for plants [34, 35].
However, to be a signal H2S needs to be perceived by plant cells and there
needs to be a response.
9
Intracellular responses to H2S have been studied and it has been found
that there are a range of effects if plant cells are so treated. For example, on
the fumigation of spinach with H2S (250 ppb: 380 g m-3) it was found that
glutathione levels increased [39], which fits well with the notion put forward by
Zhang et al. [31, 33] that H2S may impinge on oxidative stress responses. It
was estimated that approximately 40% of the H2S was converted to
glutathione in the leaves. On cessation of the fumigation glutathione levels
once again fell, with the levels being comparable to control levels after 48 h of
no H2S treatment.
Changes in glutathione will have profound effects on the intracellular
redox poise of the cells. The redox environment of proteins in cells is crucially
important for the correct functioning of many enzymes and was discussed
eloquently by Buettner and Schafer [40], and especially many proteins that
are involved in signalling [41]. It has been remarked that H2S may indeed
modulate intracellular redox status as H2S in an aqueous solution is a weak
reducing agent [42]. It was also pointed out that there was much to investigate
in this area too and that the exact impact of H2S requires further investigation.
However, at the same time that glutathione was being altered
photosynthetic carbon fixation and photosynthetic electron transport were
reported to be insensitive to the presence of H2S [37]. Fumigation of poplar
(Populus tremula X Populus alba) cuttings with H2S showed that a significant
amount of the H2S was incorporated into organic sulfur compounds. When
H2S was taken up by the leaves they had increased levels of cysteine as well
as increased levels of -glutamylcysteine synthetase. As in the spinach,
10
glutathione was also increased in poplar leaves, roots, xylem sap and phloem
exudate [43].
In another study adenosine 5’-phosphosulfate reductase (APR) was
found to be highly inhibited by the short term exposure of shoots of Brassica
oleracea L. (curly kale) to atmospheric H2S at 0.2-0.8 uL L-1 [44], although
roots of these plants were not affected. Other enzymes assayed were ATPsulfurylase (ATPS), serine acetyltransferase (SAT) and Oacetylserine(thiol)lyase (OAS-TL), but none of these appeared to be affected
by the H2S treatment. However, in the shoots of these plants the thiol content
increased. This included increases in the level of cysteine, with thiols
increasing 3 fold after 5 days exposure to H2S.
Thiols were also a focus of a study by Riemenschneider et al. [45].
Using the model plant Arabidopsis exposures of up to 48 h to atmospheric
H2S caused significant increases in both cysteine and glutathione levels.
Further work in this paper reported on the levels of encoding messenger
RNAs and levels and activities of enzymes involved in cysteine metabolism.
The activity of 3-mercaptopyruvate sulfurtransferase was only slightly higher
after the longest exposure to H2S while the activities of other enzymes which
could either remove H2S, O-acetyl-l-serine(thiol)lyase, or generate H2S, Lcysteine desulfhydrase, were not significantly affected by the H2S treatment.
Low levels of H2S (up to 0.5 microL L-1) induced an increase in the levels of
the encoding messenger RNAs for and higher protein levels of such enzymes,
but high concentrations (0.75 microL L-1) of H2S were seen to have the
opposite effect.
11
Alcohol dehydrogenase activity in plants cells was found to be inhibited
by H2S [14] in a study which used from 0.5 mM up to 4 mM. This was
accompanied by a decrease in the levels of total adenine nucleotides in the
root and also decreased nitrogen uptake and leaf growth. Alcohol
dehydrogenase is found to be an enzyme which is sensitive to both ROS [46]
and NO [47], again suggesting an interplay between H2S, ROS and NO
metabolism.
H2S was found to promote adventitious roots formation. The H2S donor
NaSH caused an increase in endogenous H2S, NO and indole acetic acid
(IAA) in shoot tips of sweet potato seedlings suggesting that H2S is acting
upstream of both IAA and NO in signalling pathways [48].
Although the transpiration rates of several species of plants including
maize, pumpkins and spinach were unaffected by short-term exposure to
atmospheric H2S, recent work [49] found that H2S caused stomatal opening in
Arabidopsis [50]. Using Arabidopsis thaliana as a model system, H2Smediated opening was seen in plants treated with either NaSH or with the H2S
donor, GYY4137 [51-53]. If leaves were not pre-opened in the light, the
effects of both NaSH and GYY4137 were seen to be more pronounced.
Furthermore, when endogenous nitric oxide was measured using a NO
sensitive probe (DAF2-DA: [54]) in conjunction with confocal microscopy, it
appeared that NO levels were lower in guard cells after treatment with either
NaSH or GYY4137, suggesting that H2S interferers with NO signalling,
perhaps through a scavenging role. However, this is not consistent with the
findings of Zhang et al. [48] who found that a H2S donor increased NO
accumulation in roots and suggested that H2S was upstream of NO in a
12
signaling pathway. Furthermore, Lamattina and Garcia-Mata [55] found that
both H2S donors NaSH and GY4137 caused stomatal closure in Vicia faba,
Arabidopsis thaliana and Impatiens walleriana. The ABC transport inhibitor
glibenclamide impaired the effect, as did the inhibitor propargylglycine which
effects cystathione  lyase and L-Cys desulfhydrase, enzymes which may be
responsible for H2S synthesis. They suggested that H2S partakes in the ABA
signaling pathway in guard cells. Therefore, there is conflicting evidence as to
the effect of H2S on guard cells. However, such contrary evidence has been
seen with other signals in stomatal regulation. Tanaka et al. [56] reported that
ethylene inhibited ABA-induced stomatal closure and some considered that
ethylene mediated auxin-induced opening of stomata [57], but others
subsequently showed that ethylene caused stomatal closure [58]. Many
environmental factors clearly impinge on the exact responses recorded in
such experiments and future work performed under standardised conditions
will no doubt reveal how compounds like H2S are truly acting.
The suggestion that there is an interaction between H2S and NO is not
new [20]. It has been shown in animal systems that H2S inhibits nitric oxide
synthase (NOS) isoforms, probably through an interaction between H2S and
the co-factor tetrahydrobiopterin (BH4) [59]. However, there is considerable
debate about the presence of NOS-like enzymes in plants [see 60] so this is
unlikely to be the mode of action for H2S here. Alternatively, it has been
suggested that NO and H2S react together to form novel
nitrosothiols/nitrothiol-like species which themselves may have cellular effects
[61].
13
However a note of caution should be added here. Several studies [for
example 50 and 55] used H2S donors such as NaSH and GY4137.
Concentrations of these are given in papers but the exact release of H2S into
solution and to which the cells are exposed is not known or indeed measured.
Therefore such studies are hard to compare to others when the role of H2S as
a signal or simply as a phytotoxin are being discussed.
If H2S is indeed acting as a signal, then it would need to be removed
when no longer required. Tobacco plants transformed with a gene for Oacetylserine lyase were more resistant to H2S treatment, suggesting that this
enzyme was used in its removal and detoxification [62, 63].
Conclusion
For hydrogen sulfide to be considered a signalling molecule in plants it needs
to have a way of being generated as and when needed, to be perceived and
to elicit a response. It has been shown that desulfhydrases are able to make
H2S, that H2S can be measured both intracellularly and extracellularly and that
many physiological and biochemical responses occur as a result of the
presence of H2S. It appears to be implicated in the transduction pathways of
several other cellular signals including ABA, auxin and NO. Future work will
no doubt confirm the place of H2S as a true cellular signal in plants,
delineating the effects of H2S as simply a phytotoxin and putting it alongside
nitric oxide, ROS and other small molecules used by plants to regulate their
cellular activities.
14
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Figure legend
Figure 1
An overview of hydrogen sulfide as a signaling molecule. It can be present in
the environment, be produced by plant cells, be removed by cells and there
are numerous effects and responses.
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